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Listening Carefully: Increased Perceptual Acuity for Species Discrimination in Multispecies Signalling Assemblages

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Listening Carefully: Increased Perceptual Acuity for Species Discrimination in Multispecies Signalling Assemblages Animal Behaviour 101 (2015) 141e154 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav Listening carefully: increased perceptual acuity for species discrimination in multispecies signalling assemblages * Anna Bastian , David S. Jacobs Department of Biological Sciences, University of Cape Town, Cape Town, South Africa article info Communication is a fundamental component of evolutionary change because of its role in mate choice Article history: and sexual selection. Acoustic signals are a vital element of animal communication and sympatric species Received 1 August 2014 may use private frequency bands to facilitate intraspecific communication and identification of con- Initial acceptance 23 September 2014 specifics (acoustic communication hypothesis, ACH). If so, animals should show increasing rates of Final acceptance 11 November 2014 misclassification with increasing overlap in frequency between their own calls and those used by Published online sympatric heterospecifics. We tested this on the echolocation of the horseshoe bat, Rhinolophus capensis, MS. number: 14-00625R using a classical habituationedishabituation experiment in which we exposed R. capensis from two phonetic populations to echolocation calls of sympatric and allopatric horseshoe bat species (Rhinolophus Keywords: clivosus and Rhinolophus damarensis) and different phonetic populations of R. capensis. As predicted by acoustic assemblages the ACH, R. capensis from both test populations were able to discriminate between their own calls and acoustic communication calls of the respective sympatric horseshoe bat species. However, only bats from one test population acoustic communication hypothesis fi bats were able to discriminate between calls of allopatric heterospeci cs and their own population when both echolocation were using the same frequency. The local acoustic signalling assemblages (ensemble of signals from functional extension sympatric conspecifics and heterospecifics) of the two populations differed in complexity as a result of habituationedishabituation contact with other phonetic populations and sympatric heterospecifics. We therefore propose that a receivers' perception acuity hierarchy of discrimination ability has evolved within the same species. Frequency alone may be suffi- Rhinolophus cient to assess species membership in relatively simple acoustic assemblages but the ability to use species discrimination additional acoustic cues may have evolved in more complex acoustic assemblages to circumvent mis- identifications as a result of the use of overlapping signals. When the acoustic signal design is under strong constraints as a result of dual functions and the available acoustic space is limited because of co- occurring species, species discrimination is mediated through improved sensory acuity in the receiver. © 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. Communication plays a crucial role in almost all aspects of an originate and are modified over evolutionary time is therefore animal's life (e.g. Maynard Smith & Harper, 2003) and is especially crucial to our understanding of the processes that generate biodi- important for species discrimination (Bradbury & Vehrencamp, versity (Mendelson & Shaw, 2012). It is likely that communication 2011; Ryan & Rand, 1993). It transmits information within a spe- systems evolved from systems used for other purposes (Monteiro & cies as well as across species and may have evolved as a product of Podlaha, 2009; Tinbergen, 1952), such as the function of feathers species coexistence (Li et al., 2013). Discriminating species is first used for insulation being extended so that they also function as important in interactions with heterospecifics allowing identifica- visual signals, for example in courtship displays (Cowen, 2005). tion of competitors, predators and prey, whereas the recognition of Particularly, knowledge of processes involved in the evolution of conspecifics is a prerequisite for any species-specific interactions, dual functions for a single trait can provide insight into how especially for mate choice (Jones, 1997; Sandoval, Mendez, & phenotypic diversity in both form and function is generated from Mennill, 2013; Slabbekoorn & Smith, 2002; Wilkins, Seddon, & existing variation. Safran, 2013). Understanding how communication signals Echolocation may provide us with an opportunity to investigate such functional extension of a trait. Echolocation is primarily used for orientation and food acquisition in echolocating bats, birds and & & * whales (Brinkløv, Fenton, Ratcliffe, 2013; Schnitzler, Moss, Correspondence: A. Bastian, UCT, Upper Campus, Private Bag X3, Rondebosch, & 7701, Cape Town, South Africa. Denzinger, 2003; Thomas, Moss, Vater, 2004) but there is E-mail address: [email protected] (A. Bastian). increasing evidence that it also functions as a means of http://dx.doi.org/10.1016/j.anbehav.2014.12.010 0003-3472/© 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. 142 A. Bastian, D. S. Jacobs / Animal Behaviour 101 (2015) 141e154 communication (Gregg, Dudzinski, & Smith, 2007; Jones & Siemers, 1989; Jacobs et al., 2007; Kingston, Jones, Zubaid, & Kunz, 2000; 2010). In the context of species discrimination, communication Kingston & Rossiter, 2004; Russo et al., 2007). This acoustic diver- cues have to be unambiguous and represent a reliable badge for the gence among signallers has also been found in morphologically species. Such species-specific cues are present in the vocalizations cryptic species living in sympatry (Guillen, Juste, & Ibanez,~ 2000; of many animal groups including insects, anurans, birds and Jones & Siemers, 2010; Jones & Van Parijs, 1993; Kingston et al., mammals (primates: Seyfarth, Cheney, & Marler, 1980; anurans: 2001; Thabah et al., 2006). However, a test of the ACH would also Duellman & Pyles, 1983; birds: Catchpole & Slater, 2008; insects: have to incorporate an investigation of the perception and Pennetier, Warren, Dabire, Russell, & Gibson, 2010). Vocalizations discrimination ability of the receiver. are often a crucial signal in mate choice (Anderson, Ambrose, In this study we used the horseshoe bat, Rhinolophus capensis,to Bearder, Dixon, & Pullen, 2000; Braune, Schmidt, & Zimmermann, investigate the role of echolocation in communication in the 2008; Charlton, Huang, & Swaisgood, 2009; Vannoni & context of the ACH. We chose a classical habituationedishabitua- Mcelligott, 2007) as they can provide information about the tion experiment (Eimas, Siqueland, Jusczyk, & Vigorito, 1971)in sender which is used by the receiver to evaluate the mate's inten- which we exposed R. capensis to recorded calls of two sympatric tion, compatibility and quality. The voice of mammals, for example, horseshoe bat species (Rhinolophus clivosus and Rhinolophus dam- is often an honest cue which allows an individual to assess the body arensis) and different phonetic populations of R. capensis. In these size or mass of the sender (Fitch, 2006; Liebermann & Blumstein, assemblages we have populations of the same species using 1991). Among echolocating mammals bats are ideal candidates different echolocation frequencies as well as different hetero- for studies on echolocation in the context of communication specifics using overlapping frequencies. This natural system pro- because most species form groups with complex social structures vides an excellent opportunity to test whether R. capensis (Kulzer, 2005) in which many interactions are managed by acoustic discriminates between different species and populations on the signals (Altringham & Fenton, 2003; Fenton, 1985). The acoustic basis of their echolocation calls. If acoustic divergence in the structure of their echolocation calls has a complex frequencyetime echolocation frequencies of R. capensis is a result of selection contour and there are many different types of calls (Maltby, Jones, & favouring the use of private frequency bands as proposed by the Jones, 2010) providing sufficient variation to encode multiple cues. ACH, R. capensis should show increasing rates of misclassification Furthermore, echolocation calls contain diagnostic information with increasing overlap between its own calls and those used by about the sender which can be useful for others and, as a frequently sympatric heterospecifics. This concomitantly means that in- available signal, echolocation transmits information free of addi- dividuals of R. capensis from the different phonetic populations tional costs to a receiver (Dechmann, Wikelski, Noordwijk, Voigt, & should have difficulty recognizing each other as belonging to the Voigt-Heucke, 2013). In echolocating bats, the relationship be- same species if they use calls of dissimilar frequency. In addition tween echolocation call frequency and body size is well established this system allows us to test whether peak frequency is the only (Jacobs, Barclay, & Walker, 2007; Jones, 1999), and echolocation parameter used by bats to discriminate between species. calls often carry species-specific signatures, individual signatures, population-specific signatures and sex-specific signatures (Jones & METHODS Siemers, 2010). Several recent playback studies have provided evidence that Study Animal conspecific bats are able to extract information encoded in the echolocation calls of other bats such as species membership, fa- Rhinolophus capensis (Cape horseshoe bat) has a wide distribu- miliarity and sex (Dorado Correa, Goerlitz,
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